Plasma membrane calcium ATPases are important components of receptor-mediated signaling in plant immune responses and development.

N. Frei dit Frey, M. Mbengue, M.A.C.J. Kwaaitaal, L.M.C. Nitsch, D. Altenbach, H. Häweker, R. Lozano-Duran, M.F. Njo, T. Beeckman, B. Huettel, J.W. Borst, R. Panstruga, S. Robatzek

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Abstract

Plasma membrane-resident receptor kinases (RKs) initiate signaling pathways important for plant immunity and development. In Arabidopsis (Arabidopsis thaliana), the receptor for the elicitor-active peptide epitope of bacterial flagellin, flg22, is encoded by FLAGELLIN SENSING2 (FLS2), which promotes plant immunity. Despite its relevance, the molecular components regulating FLS2-mediated signaling remain largely unknown. We show that plasma membrane ARABIDOPSIS-AUTOINHIBITED Ca2+-ATPase (ACA8) forms a complex with FLS2 in planta. ACA8 and its closest homolog ACA10 are required for limiting the growth of virulent bacteria. One of the earliest flg22 responses is the transient increase of cytosolic Ca2+ ions, which is crucial for many of the well-described downstream responses (e.g. generation of reactive oxygen species and the transcriptional activation of defense-associated genes). Mutant aca8 aca10 plants show decreased flg22-induced Ca2+ and reactive oxygen species bursts and exhibit altered transcriptional reprogramming. In particular, mitogen-activated protein kinase-dependent flg22-induced gene expression is elevated, whereas calcium-dependent protein kinase-dependent flg22-induced gene expression is reduced. These results demonstrate that the fine regulation of Ca2+ fluxes across the plasma membrane is critical for the coordination of the downstream microbe-associated molecular pattern responses and suggest a mechanistic link between the FLS2 receptor complex and signaling kinases via the secondary messenger Ca2+. ACA8 also interacts with other RKs such as BRI1 and CLV1 known to regulate plant development, and both aca8 and aca10 mutants show morphological phenotypes, suggesting additional roles for ACA8 and ACA10 in developmental processes. Thus, Ca2+ ATPases appear to represent general regulatory components of RK-mediated signaling pathways.
Original languageEnglish
Pages (from-to)798-809
JournalPlant Physiology
Volume159
Issue number2
DOIs
Publication statusPublished - 2012

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Plasma Membrane Calcium-Transporting ATPases
Plant Immunity
Ca2-transporting ATPase
Phosphotransferases
plasma membrane
immune response
calcium
phosphotransferases (kinases)
receptors
Plant Development
Calcium-Transporting ATPases
Cell Membrane
Arabidopsis
Reactive Oxygen Species
reactive oxygen species
Flagellin
Gene Expression
immunity
Mitogen-Activated Protein Kinases
flagellin

Keywords

  • pattern-recognition receptors
  • arabidopsis-thaliana
  • innate immunity
  • molecular-patterns
  • protein-kinases
  • nadph oxidase
  • cell-death
  • defense
  • bak1
  • brassinosteroids

Cite this

Frei dit Frey, N. ; Mbengue, M. ; Kwaaitaal, M.A.C.J. ; Nitsch, L.M.C. ; Altenbach, D. ; Häweker, H. ; Lozano-Duran, R. ; Njo, M.F. ; Beeckman, T. ; Huettel, B. ; Borst, J.W. ; Panstruga, R. ; Robatzek, S. / Plasma membrane calcium ATPases are important components of receptor-mediated signaling in plant immune responses and development. In: Plant Physiology. 2012 ; Vol. 159, No. 2. pp. 798-809.
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abstract = "Plasma membrane-resident receptor kinases (RKs) initiate signaling pathways important for plant immunity and development. In Arabidopsis (Arabidopsis thaliana), the receptor for the elicitor-active peptide epitope of bacterial flagellin, flg22, is encoded by FLAGELLIN SENSING2 (FLS2), which promotes plant immunity. Despite its relevance, the molecular components regulating FLS2-mediated signaling remain largely unknown. We show that plasma membrane ARABIDOPSIS-AUTOINHIBITED Ca2+-ATPase (ACA8) forms a complex with FLS2 in planta. ACA8 and its closest homolog ACA10 are required for limiting the growth of virulent bacteria. One of the earliest flg22 responses is the transient increase of cytosolic Ca2+ ions, which is crucial for many of the well-described downstream responses (e.g. generation of reactive oxygen species and the transcriptional activation of defense-associated genes). Mutant aca8 aca10 plants show decreased flg22-induced Ca2+ and reactive oxygen species bursts and exhibit altered transcriptional reprogramming. In particular, mitogen-activated protein kinase-dependent flg22-induced gene expression is elevated, whereas calcium-dependent protein kinase-dependent flg22-induced gene expression is reduced. These results demonstrate that the fine regulation of Ca2+ fluxes across the plasma membrane is critical for the coordination of the downstream microbe-associated molecular pattern responses and suggest a mechanistic link between the FLS2 receptor complex and signaling kinases via the secondary messenger Ca2+. ACA8 also interacts with other RKs such as BRI1 and CLV1 known to regulate plant development, and both aca8 and aca10 mutants show morphological phenotypes, suggesting additional roles for ACA8 and ACA10 in developmental processes. Thus, Ca2+ ATPases appear to represent general regulatory components of RK-mediated signaling pathways.",
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author = "{Frei dit Frey}, N. and M. Mbengue and M.A.C.J. Kwaaitaal and L.M.C. Nitsch and D. Altenbach and H. H{\"a}weker and R. Lozano-Duran and M.F. Njo and T. Beeckman and B. Huettel and J.W. Borst and R. Panstruga and S. Robatzek",
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Frei dit Frey, N, Mbengue, M, Kwaaitaal, MACJ, Nitsch, LMC, Altenbach, D, Häweker, H, Lozano-Duran, R, Njo, MF, Beeckman, T, Huettel, B, Borst, JW, Panstruga, R & Robatzek, S 2012, 'Plasma membrane calcium ATPases are important components of receptor-mediated signaling in plant immune responses and development.', Plant Physiology, vol. 159, no. 2, pp. 798-809. https://doi.org/10.1104/pp.111.192575

Plasma membrane calcium ATPases are important components of receptor-mediated signaling in plant immune responses and development. / Frei dit Frey, N.; Mbengue, M.; Kwaaitaal, M.A.C.J.; Nitsch, L.M.C.; Altenbach, D.; Häweker, H.; Lozano-Duran, R.; Njo, M.F.; Beeckman, T.; Huettel, B.; Borst, J.W.; Panstruga, R.; Robatzek, S.

In: Plant Physiology, Vol. 159, No. 2, 2012, p. 798-809.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Plasma membrane calcium ATPases are important components of receptor-mediated signaling in plant immune responses and development.

AU - Frei dit Frey, N.

AU - Mbengue, M.

AU - Kwaaitaal, M.A.C.J.

AU - Nitsch, L.M.C.

AU - Altenbach, D.

AU - Häweker, H.

AU - Lozano-Duran, R.

AU - Njo, M.F.

AU - Beeckman, T.

AU - Huettel, B.

AU - Borst, J.W.

AU - Panstruga, R.

AU - Robatzek, S.

PY - 2012

Y1 - 2012

N2 - Plasma membrane-resident receptor kinases (RKs) initiate signaling pathways important for plant immunity and development. In Arabidopsis (Arabidopsis thaliana), the receptor for the elicitor-active peptide epitope of bacterial flagellin, flg22, is encoded by FLAGELLIN SENSING2 (FLS2), which promotes plant immunity. Despite its relevance, the molecular components regulating FLS2-mediated signaling remain largely unknown. We show that plasma membrane ARABIDOPSIS-AUTOINHIBITED Ca2+-ATPase (ACA8) forms a complex with FLS2 in planta. ACA8 and its closest homolog ACA10 are required for limiting the growth of virulent bacteria. One of the earliest flg22 responses is the transient increase of cytosolic Ca2+ ions, which is crucial for many of the well-described downstream responses (e.g. generation of reactive oxygen species and the transcriptional activation of defense-associated genes). Mutant aca8 aca10 plants show decreased flg22-induced Ca2+ and reactive oxygen species bursts and exhibit altered transcriptional reprogramming. In particular, mitogen-activated protein kinase-dependent flg22-induced gene expression is elevated, whereas calcium-dependent protein kinase-dependent flg22-induced gene expression is reduced. These results demonstrate that the fine regulation of Ca2+ fluxes across the plasma membrane is critical for the coordination of the downstream microbe-associated molecular pattern responses and suggest a mechanistic link between the FLS2 receptor complex and signaling kinases via the secondary messenger Ca2+. ACA8 also interacts with other RKs such as BRI1 and CLV1 known to regulate plant development, and both aca8 and aca10 mutants show morphological phenotypes, suggesting additional roles for ACA8 and ACA10 in developmental processes. Thus, Ca2+ ATPases appear to represent general regulatory components of RK-mediated signaling pathways.

AB - Plasma membrane-resident receptor kinases (RKs) initiate signaling pathways important for plant immunity and development. In Arabidopsis (Arabidopsis thaliana), the receptor for the elicitor-active peptide epitope of bacterial flagellin, flg22, is encoded by FLAGELLIN SENSING2 (FLS2), which promotes plant immunity. Despite its relevance, the molecular components regulating FLS2-mediated signaling remain largely unknown. We show that plasma membrane ARABIDOPSIS-AUTOINHIBITED Ca2+-ATPase (ACA8) forms a complex with FLS2 in planta. ACA8 and its closest homolog ACA10 are required for limiting the growth of virulent bacteria. One of the earliest flg22 responses is the transient increase of cytosolic Ca2+ ions, which is crucial for many of the well-described downstream responses (e.g. generation of reactive oxygen species and the transcriptional activation of defense-associated genes). Mutant aca8 aca10 plants show decreased flg22-induced Ca2+ and reactive oxygen species bursts and exhibit altered transcriptional reprogramming. In particular, mitogen-activated protein kinase-dependent flg22-induced gene expression is elevated, whereas calcium-dependent protein kinase-dependent flg22-induced gene expression is reduced. These results demonstrate that the fine regulation of Ca2+ fluxes across the plasma membrane is critical for the coordination of the downstream microbe-associated molecular pattern responses and suggest a mechanistic link between the FLS2 receptor complex and signaling kinases via the secondary messenger Ca2+. ACA8 also interacts with other RKs such as BRI1 and CLV1 known to regulate plant development, and both aca8 and aca10 mutants show morphological phenotypes, suggesting additional roles for ACA8 and ACA10 in developmental processes. Thus, Ca2+ ATPases appear to represent general regulatory components of RK-mediated signaling pathways.

KW - pattern-recognition receptors

KW - arabidopsis-thaliana

KW - innate immunity

KW - molecular-patterns

KW - protein-kinases

KW - nadph oxidase

KW - cell-death

KW - defense

KW - bak1

KW - brassinosteroids

U2 - 10.1104/pp.111.192575

DO - 10.1104/pp.111.192575

M3 - Article

VL - 159

SP - 798

EP - 809

JO - Plant Physiology

JF - Plant Physiology

SN - 0032-0889

IS - 2

ER -